Comparison of the Glucocorticoid Concentrations between Three Species of Lemuridae Kept in a Temporary Housing Facility
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
PubMed
32532091
PubMed Central
PMC7341240
DOI
10.3390/ani10061013
PII: ani10061013
Knihovny.cz E-zdroje
- Klíčová slova
- enzyme immunoassay, faecal analysis, glucocorticoid metabolites, non-invasive, zoo,
- Publikační typ
- časopisecké články MeSH
We compared the glucocorticoid concentrations in response to various types of potential stressors present during standard operation of a temporary housing facility between three species, namely, ring-tailed lemurs, collared brown lemurs and white-headed lemurs. The levels of faecal glucocorticoid metabolites (FGMs) were measured non-invasively on a daily basis during a 30-day period. A total of 510 faecal samples were collected. Concentrations of immunoreactive glucocorticoid hormone metabolites were measured in the obtained extracts by using an enzyme immunoassay. The polyclonal antibodies used in this assay were directed against the metabolite 11-oxo-etiocholanolone I. We found all three monitored lemur species to respond to specific potentially stressful situations by increasing (p < 0.05) the FGM levels within one to two days after the event. Although housed in the same room, differences in response to potentially stressful situations were found in white-headed lemurs compared to ring-tailed lemurs. Increased mean levels of the FGMs were found more frequently in white-headed lemurs than in ring-tailed lemurs. The results suggest that this species may be more sensitive to changes in its surroundings. In general, the levels of the FGMs showed a similar pattern during 30 days of monitoring suggesting that all groups of lemurs responded in a similar manner to the same events. However, we recorded the differences in the absolute values of glucocorticoid concentrations between the monitored species likely due to the differences in sex ratios in the groups and presence of lactating females in the ring-tailed lemurs.
Zobrazit více v PubMed
Möstl E., Palme R. Hormones as indicators of stress. Domest. Anim. Endocrinol. 2002;23:67–74. doi: 10.1016/S0739-7240(02)00146-7. PubMed DOI
Morgan K.N., Tromborg C.H.T. Sources of stress in captivity. Appl. Anim. Behav. Sci. 2007;102:262–302. doi: 10.1016/j.applanim.2006.05.032. DOI
Pribbenow S., Jewgenow K., Vargas A., Rodrigo S., Naidenko S., Dehnhard M. Validation of an enzyme immunoassay for the measurement of faecal glucocorticoid metabolites in Eurasian (Lynx lynx) and Iberian lynx (Lynx pardinus) Gen. Comp. Endocrinol. 2014;206:166–177. doi: 10.1016/j.ygcen.2014.07.015. PubMed DOI
Bashaw M.J., Sicks F., Palme R., Schwarzenberger F., Tordiffe A.S.W., Ganswindt A. Non-invasive assessment of adrenocortical activity as a measure of stress in giraffe (Giraffa camelopardalis) BMC Vet. Res. 2016;235:1–13. doi: 10.1186/s12917-016-0864-8. PubMed DOI PMC
Palme R., Rettenbacher S., Touma C., El-Bahr S.M., Möstl E. Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples. Ann. NY Acad. Sci. 2005;1040:162–171. doi: 10.1196/annals.1327.021. PubMed DOI
Palme R. Non-invasive measurement of glucocorticoids: Advances and problems. Physiol. Behav. 2019;199:229–243. doi: 10.1016/j.physbeh.2018.11.021. PubMed DOI
Touma C., Palme R. Measuring fecal glucocorticoid metabolites in mammals and birds: The importance of validation. Ann. NY Acad. Sci. 2005;1046:54–74. doi: 10.1196/annals.1343.006. PubMed DOI
Touma C., Palme R., Sachser N. Analyzing corticosterone metabolites in fecal samples of mice: A noninvasive technique to monitor stress hormones. Horm. Behav. 2004;45:10–22. doi: 10.1016/j.yhbeh.2003.07.002. PubMed DOI
Palme R. Measuring fecal steroids: Guidelines for practical application. Ann. NY Acad. Sci. 2005;1046:75–80. doi: 10.1196/annals.1343.007. PubMed DOI
Millspaugh J.J., Washburn B.E. Use of fecal glucocorticoid metabolite measures in conservation biology research: Considerations for application and interpretation. Gen. Comp. Endocrinol. 2004;138:189–199. doi: 10.1016/j.ygcen.2004.07.002. PubMed DOI
Mason G., Mendl M. Why is there no simple way of measuring animal welfare? Anim. Welf. 1993;2:301–319.
Mason G.J. Species differences in responses to captivity: Stress, welfare and the comparative method. Trends Ecol. Evol. 2010;25:713–721. doi: 10.1016/j.tree.2010.08.011. PubMed DOI
Weingrill T., Willems E.P., Zimmermann N., Steinmetz H., Heistermann M.M. Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.) Gen. Comp. Endocrinol. 2011;172:446–457. doi: 10.1016/j.ygcen.2011.04.008. PubMed DOI
Cocks L. Factors affecting mortality, fertility, and well-being in relation to species differences in captive orangutans. Int. J. Primatol. 2007;28:421–428. doi: 10.1007/s10764-007-9116-x. DOI
Campbell J.L., Eisemann J.H., Williams C.V., Glenn K.M. Description of the gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am. J. Primatol. 2000;52:133–142. doi: 10.1002/1098-2345(200011)52:3<133::AID-AJP2>3.0.CO;2-#. PubMed DOI
Balestri M., Barresi M., Campera M., Serra V., Ramanamanjato J.B., Heistermann M., Donati G. Habitat degradation and seasonality affect physiological stress levels of Eulemur collaris in littoral forest fragments. PLoS ONE. 2014;9:e107698. doi: 10.1371/journal.pone.0107698. PubMed DOI PMC
Ostner J., Kappeler P., Heistermann M. Androgen and glucocorticoid levels reflex seasonally occurring social challenges in male red fronted lemurs (Eulemur fulvus rufus) Behav. Ecol. Sociobiol. 2008;62:627–638. doi: 10.1007/s00265-007-0487-y. PubMed DOI PMC
Volfova M., Machovcova Z., Schwarzenberger F., Voslarova E., Bedanova I., Vecerek V. Non-invasive assessment of adrenocortical activity as a measure of stress in ring-tailed lemurs (Lemur catta) Berl. Munch. Tierarztl. Wochenschr. 2020;133:28–35.
Volfova M., Machovcova Z., Schwarzenberger F., Voslarova E., Bedanova I., Vecerek V. The effects of transport stress on the behaviour and adrenocortical activity of the black-and-white ruffed lemur (Varecia variegata) Acta Vet. Brno. 2019;88:85–92. doi: 10.2754/avb201988010085. DOI
Cockrem J.F. Individual Variation in Glucocorticoid Stress Responses in Animals. Gen. Comp. Endocrinol. 2013;181:45–58. doi: 10.1016/j.ygcen.2012.11.025. PubMed DOI
Heistermann M., Palme R., Ganswindt A. Comparison of different enzyme immunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am. J. Primatol. 2006;68:257–273. doi: 10.1002/ajp.20222. PubMed DOI
Clark F.E., Fitzpatrick M., Hartley A., King A.J., Lee T., Routh A., Walker S.L., George K. Relationship between behavior, adrenal activity, and environment in zoo-housed Western lowland gorillas (Gorilla gorilla gorilla) Zoo Biol. 2011;30:1–16. doi: 10.1002/zoo.20396. PubMed DOI
Pirovino M., Heistermann M., Zimmermann N., Zingg R., Clauss M., Codron D., Kauphanspeter F.J., Steinmetz W. Fecal glucocorticoid measurements and their relation to rearing, behavior, and environmental factors in the population of pileated gibbons (Hylobates pileatus) held in European zoos. Int. J. Primatol. 2011;32:1161–1178. doi: 10.1007/s10764-011-9532-9. DOI
Hämäläinen A., Heistermann M., Fenosoa Z.S.E., Raus C. Evaluating capture stress in wild gray mouse lemurs via repeated fecal sampling: Method validation and the influence of prior experience and handling protocols on stress responses. Gen. Comp. Endocrinol. 2014;195:68–79. doi: 10.1016/j.ygcen.2013.10.017. PubMed DOI
Palme R., Touma C., Arias N., Dominchin M.F., Lepschy M. Steroid extraction: Get the best out of faecal samples. Wien. Tierarztl. Monatsschr. 2013;100:238–246.
Palme R., Möstl E. Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. Mamm. Biol. 1997;62:192–197.
Zar J.H. Biostatistical Analysis. 4th ed. Prentice-hall, INC; New Jersey, NJ, USA: 1999.
Grandin T. Assessment of stress during handling and transport. Sci. J. Anim. Sci. 1997;75:249–257. doi: 10.2527/1997.751249x. PubMed DOI
Margulis S.W., Hoyos C., Anderson M. Effect of felid activity on zoo visitor interest. Zoo Biol. 2003;22:587–599. doi: 10.1002/zoo.10115. DOI
Romano M.C., Rodas A.Z., Valdez R.A., Hernández S.E., Galindo F., Canale D., Brousset D.M. Stress in wildlife species: Noninvasive monitoring of glucocorticoids. Neuroimmunomodulation. 2010;17:209–212. doi: 10.1159/000258726. PubMed DOI
Owen M.A., Swaisgood R.R., Czekala N.M., Steinman K., Lindburg D.G. Monitoring stress in captive giant pandas (Ailuropoda melanoleuca): Behavioral and hormonal responses to ambient noise. Zoo Biol. 2004;23:147–164. doi: 10.1002/zoo.10124. DOI
Cavigelli S.A. Behavioural patterns associated with faecal cortisol levels in free rating female Ring-tailed lemurs, Lemur catta. Anim. Behav. 1999;57:935–944. doi: 10.1006/anbe.1998.1054. PubMed DOI
Cavigelli S.A., Dubovick T., Levash W., Jolly A., Pitts A. Female dominance status and fecal corticoids in a kooperative breeder with low reproductive skew: Ring-Tailed lemurs (Lemur catta) Horm. Behav. 2003;43:166–179. doi: 10.1016/S0018-506X(02)00031-4. PubMed DOI
Gould L., Ziegler T.E., Wittwer D.J. Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Nahafaly Reserve, Madagascar. Am. J. Primatol. 2005;67:5–23. doi: 10.1002/ajp.20166. PubMed DOI
Bennett K.A., Moss S.E.W., Pomeroy P., Speakman J.R., Fedak M.A. Effects of handling regime and sex on changes in cortisol, thyroid hormones and body mass in fasting grey seal pups. Comp. Biochem. Phys. A. 2012;161:69–76. doi: 10.1016/j.cbpa.2011.09.003. PubMed DOI
McGillivray C.L. Husbandry Manual for Black and Ehite Ruffed Lemur—Varecia variegata variegata (Mammalia: Lemuridae) Western Sydney Institute of Tafe; Richmond, Australia: 2007.
Quine H. Husbandry Guidelines for White Fronted Brown Lemur (Eulemur fulvus albifrons) Western Sydney Institute of Tafe; Richmond, Australia: 2009.
Balcombe J.P., Barnard N.D., Sandusky C. Laboratory routines cause animal stress. J. Am. Assoc. Lab. Anim. Sci. 2004;43:42–51. PubMed
Rangel-Negrín A., Flores-Escobar E., Chavira R., Canales-Espinosa D., Dias P.A.D. Physiological and analytical validations of fecal steroid hormone measures in black howler monkeys. Primates. 2014;55:459–465. doi: 10.1007/s10329-014-0432-4. PubMed DOI
Snyder R.J., Perdue B.M., Powell D.M., Forthman D.L., Bloomsmith M.A., Maple T.L. Behavioral and hormonal consequences of transporting giant pandas from China to the United states. J. Appl. Anim. Welf. Sci. 2012;15:1–20. doi: 10.1080/10888705.2012.624046. PubMed DOI
Shutt K., Setchell J.M., Heistermann M. Non-invasive monitoring of physiological stress in the estern lowland gorila (Gorilla gorilla gorilla): Validation of fecal glucocorticoid assay and methods for practical application in the field. Gen. Comp. Endocrinol. 2012;179:167–177. doi: 10.1016/j.ygcen.2012.08.008. PubMed DOI
Boccia M.L., Laudenslager M.L., Reite M.L. Individual differences in Macaques’ responses to stressors based on social and physiological factors: Implications for primate welfare and research outcomes. Lab. Anim. 1995;29:250–257. doi: 10.1258/002367795781088315. PubMed DOI
Wasser S.K., Hunt K.E., Brown J.L., Cooper K., Crockett C.M., Bechert U., Millspaugh J.J., Larson S., Monfort S.L. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 2000;120:260–275. doi: 10.1006/gcen.2000.7557. PubMed DOI
Cavigelli S.A., Caruso M.J. Sex, social status and physiological stress in primates: The importace of social and glucocorticoid dynamics. Philos. Trans. R. Soc. 2015;370:1–13. doi: 10.1098/rstb.2014.0103. PubMed DOI PMC
Starling A.P., Charpentier M.J.E., Fitzpatrick C., Scordato E.S., Drea C.H.M. Seasonality, sociality, and reproduction: Long-Term stressors of ring-tailed lemurs (Lemur catta) Horm. Behav. 2010;57:76–85. doi: 10.1016/j.yhbeh.2009.09.016. PubMed DOI
Arias N., Requena M., Palme R. Measuring faecal glucocorticoid metabolites as a non-invasive tool for monitoring adrenocortical activity in South american camelids. Anim. Welf. 2013;22:25–31. doi: 10.7120/09627286.22.1.025. DOI
Dantzer B., McAdam A.G., Palme R., Fletcher Q.E., Boutin S., Humphries M.M., Boonstra R. Fecal cortisol metabolite levels in free-ranging North American red squirrels: Assay validation and the effects of reproductive condition. Gen. Comp. Endocrinol. 2010;167:279–286. doi: 10.1016/j.ygcen.2010.03.024. PubMed DOI
Carrera S.C., Sen S., Heistermann M., Lu A., Beehner J.C. Low rank and primiparity increase fecal glucocorticoid metabolites across gestation in wild geladas. Gen. Comp. Endocrinol. 2020;293:113494. doi: 10.1016/j.ygcen.2020.113494. PubMed DOI
MacLean E.L., Sandel A.A., Bray J., Oldenkamp R.E., Reddy R.B., Hare B.A. Group Size Predicts Social but Not Nonsocial Cognition in Lemurs. PLoS ONE. 2013;8:e66359. doi: 10.1371/journal.pone.0066359. PubMed DOI PMC